i Systematics, Biogeography and Echolocation of Tube-nosed Bats Genus Murina (Chiroptera: Vespertilionidae) in Mainland Southeast Asia Pipat Soisook A Thesis Submitted in Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Biology Prince of Songkla University 2013 Copyright of Prince of Songkla University ii Thesis Title Systematics, biogeography and echolocation of Tube- nosed bats genus Murina (Chiroptera: Vespertilionidae) in mainland Southeast Asia Author Pipat Soisook Major Program Biology Examining Committee: Major Advisor: ………………………………………. …………………….………….Chairperson (Assoc. Prof. Dr. Chutamas Satasook) (Asst. Prof. Dr. Sara Bumrungsri) ………………………………..Committee Co-Advisor: (Assoc. Prof. Dr. Chutamas Satasook) ………………………………………. ………………………………..Committee (Dr. Paul J. J. Bates) (Dr. Paul J. J. Bates) ………………………………..Committee (Dr. Vu Dinh Thong) The Graduate School, Prince of Songkla University, has approved this thesis as partial fulfillment of the requirements for the Doctor of Philosophy in Biology ……..………………………….……….. (Assoc. Prof. Dr. Teerapol Srichana) Dean of Graduate School iii This is to certify that the work here submitted is the result of the candidate’s own investigations. Due acknowledgement has been made of any assistance received. ………………………………… Signature (Assoc. Prof. Dr. Chutamas Satasook) Major Advisor …………………………………. Signature (Pipat Soisook) Candidate iv I hereby certify that this work has not been accepted in substance for any degree, and is not being currently submitted in candidature for any degree. ………………………………. Signature (Pipat Soisook) Candidate v Thesis Title Systematics, biogeography and echolocation of Tube- nosed bats genus Murina (Chiroptera: Vespertilionidae) in mainland Southeast Asia Author Pipat Soisook Major Program Biology Academic Year 2013 ABSTRACT The Tube-nosed bat genus Murina in mainland Southeast Asia is reviewed. Eighteen species are currently recorded from the region. A new cryptic species of the ‘cyclotis-complex’ is described from peninsular Thailand based on a combination of external, craniodental and genetic differences. The population previously referred to M. cyclotis from the Nicobar Islands is described as a new subspecies of this new species. Another new species belonging to ‘suilla-group’ is described based on two specimens from the southernmost part of peninsular Thailand. M. walstoni, M. annamitica, and M. rozendaali, are recorded from Thailand for the first time. The diagnostic characters of each species are summarised and the taxonomy is discussed. DNA barcodes support current taxonomic conclusions but do not agree with traditional morphological groupings of the ‘M. cyclotis-group’ and ‘M. suilla-group’. In most cases, the pattern of distribution of Murina in mainland Southeast Asia is strongly related with the zoogeographical division between the Indochinese and Sundaic Subregions but with one exception in the case of M. huttoni. Additional data on the ecology, distribution and conservation, where available, are included and discussed. A key to the species of Murina known to occur in mainland Southeast Asia is provided. Echolocation call and social call characters were described. Results of a field experiment on the efficacy of acoustic lures strongly indicate that a harp trap with acoustic lure, AutoBat, attached have a significantly higher trapping success than normal harp trapping. A random variety of Murina species were caught in the ‘AutoBat traps’; individuals responded to all social calls not just to those of their own species. vi ACKNOWLEDGEMENTS I am deeply grateful to my thesis advisors Assoc. Prof. Dr. Chutamas Satasook and Dr. Paul J. J. Bates for their support, encouragement, guidance, proofreading and corrections on the draft of my thesis. I also grateful to the thesis examiners, Asst. Prof. Dr. Sara Bumrungsri and Dr. Vu Dinh Thong, for valuable comments and suggestions to improve this study. I am thankful to the Darwin Initiative, DEFRA, UK for a fully financial support of this study. I thank the Graduate School, PSU for financial support for fieldwork in Thailand and study visit to the UK. I am indebted to Sunate Karapan and staff of the Halabala Wildlife Research Station, as well as Prateep Rojanadilok, Mongkol Safoowong and staff of the Wildlife Research Division, of the Department of National Parks, Wildlife and Plant Conservation (DNP). Without them, fieldwork and specimens collection would not possible. I thank David Hill for loaning me the Autobat machines and suggestions in acoustic lure. I also thank Jirapan Yimkaew, Sawwalak Billasoy, Abdullah Samoh, Bounsavane Douangboubpha, Ith Saveng, as well as all students at Mammals and Birds Research Unit and all staff at the PSUNHM for their help and support during the field expeditions and with specimen preparation. I would like to thank Robert Baker, M. T. Abdullah, Faisal Anwarali Khan, Ibnu Maryanto, Vu Dinh Thong, Gabor Csorba, Neil Furey and Pichai Sonchaeng for kindly loaning me specimens under their care. I thank Evgeny Zhakarov, Alex Borisenko and Nataly Ivanova for coordinating the analyses of the DNA Barcode. Thanks also go to David Harrison, Nikky Thomas, Malcolm Pearch and Beatrix Lanzinger at the Harrison Institute, UK for their suggestions and help. I thank Tigga Kingston and Joe Chun-Chia Huang (TTU) and the Southeast Asian Bat Conservation and Research Unit (SEABCRU) for supporting networking between researchers. Special thanks go to Stephanie Beattie for her warm welcome and all her help during my stay in the UK. I am fully appreciate to Roberto Portela Miguez and staff at mammal collection and library of Natural History Museum, London, for the permission to study the bat collection. Pipat Soisook vii CONTENTS Page Contents vii List of tables x List of figures xi Chapter 1 Introduction and literature review 1 Introduction 1 General literature review 4 - Diversity and distribution 4 - Taxonomic background 4 - Ecology and conservation 7 - Echolocation 8 Chapter 2 An overview of materials and methods 9 Morphometric and morphological data 9 Additional specimens 10 Measurements 14 Acoustic data 16 Genetic data 16 Chapter 3 A review of Murina cyclotis complex with descriptions of a new species and subspecies 21 Abstract 21 Introduction 22 Materials and methods 23 Systematic descriptions 24 Chapter 4 Systematics of Murina in mainland Southeast Asia with description of a new species 55 Abstract 55 Introduction 56 viii CONTENTS (Continued) Page Materials and methods 59 Systematic descriptions 60 Genetic and biogeographic implications 104 A key to species of Murina in mainland Southeast Asia 113 Chapter 5 Echolocation call characters of Murina and the use of their socials calls in acoustic lure 115 Abstract 115 Introduction 116 Materials and methods 117 Result 121 Discussion 132 References 140 Appendix 150 Appendix 1. List of specimens examined 151 Appendix 2. List of genetic samples analysed 159 Vitae 163 ix LIST OF TABLES Table Page 3-1 External measurements (in mm) and body mass (MASS) (in gram) of M. sp. nov. [A], M. sp. [A] subsp. nov., M. cyclotis, M. fionae and M. peninsularis. Sample sizes of male and female specimens examined, mean ±SD, min–max values are given. A sample size that differs from the total number of specimens is given in brackets. Definitions of measurements are listed in the Chapter 2 50 3-2 Craniodental measurements (in mm) of M. sp. nov. [A], M. sp. [A] subsp. nov., M. cyclotis, M. fionae and M. peninsularis. Sample sizes of male and female specimens, mean ±SD; min–max values are given. A sample size that differs from the total number of specimens is given in brackets. Definitions of measurement are listed in Chapter 2 52 3-3 Factor loading scores of the characters used in Fig. 3-7 and variance explained between the first three components. Definitions of measurements are listed in Chapter 2 54 4-1 External measurements (in mm) and body mass (MASS) (in gram) of 14 species of Murina. Sample sizes of male and female specimens examined, mean ±SD, min–max values are given. A sample size that differs from the total number of specimens is given in brackets. Definitions of measurements are listed in the Chapter 2 107 4-2 Craniodental measurements (in mm) of nine species of M. suilla-group. Sample sizes of male and female specimens, mean ±SD; min–max values are given. A sample size that differs from the total number of specimens is given in brackets. Definitions of measurement are listed in Chapter 2 109 x LIST OF TABLES (Continued) Table Page 4-3 Craniodental measurements (in mm) of five species of M. cyclotis- group. Sample sizes of male and female specimens, mean ±SD; min–max values are given. A sample size that differs from the total number of specimens is given in brackets. Definitions of measurement are listed in Chapter 2 111 5-1 Mean and standard deviation (SD) of six call parameters of 10 Murina. Number of specimens (N) and number of calls analysed (n) are given 123 5-2 Summary of classification with cross validation based on six call parameters of eight Murina species by discriminant analysis. M. cyclotis and M. annamitica were excluded from the analysis because of small sample size 128 5-3 Statistical comparison of the call characters between species by Mann-Whitney U test. M. cyclotis and M. annamitica were excluded from the analysis because of small sample size. *, ** and *** represent significant differences at P < 0.05, P < 0.01 and P < 0.001, respectively. NS represents non-significant difference (P > 0.05) 133 xi LIST OF FIGURES Figures Pages 2-1 Localities where the additional field surveys were undertaken in Thailand 13 2-2 Antero-lateral view of the head of Murina and the measurements of the ear length (E) and the tragus length (TRG) 17 2-3 External measurements of Murina 18 2-4 Cranial measurements of Murina 19 2-5 Dental measurements of Murina 20 3-1 Distribution of M. sp. nov. [A] (circles), M. cyclotis (squares), M. fionae (triangles) and M. peninsularis (diamonds). The black symbols refer to specimens examined by the authors, whereas the blank symbols refer to records from literature or released individuals.